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Biology of Reproduction 61, 797-801 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.

Articles

Immunolocalization of Progesterone Receptors in Bovine Placentomes Throughout Mid and Late Gestation and at Parturition1

Gerhard Schuler2,a, Christina Wirtha, Karl Klischb, Christiane Pfarrerb, Rudolf Leiserb, and Bernd Hoffmanna

a Klinik für Geburtshilfe, Gynäkologie und Andrologie der Groß- und Kleintiere mit Tierärztlicher Ambulanz, and b Institut für Veterinär-Anatomie, -Histologie und -Embryologie, Justus-Liebig-Universität, D-35392 Giessen, Germany


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The corpus luteum is the main source of progesterone (P4) responsible for maintenance of gestation in cattle. So far it has not been possible to assign any biological role to placental P4, which contributes only marginally and temporarily to peripheral maternal blood levels. In order to identify possible P4 target cells within the placenta, placentomes from 150-, 220-, 240-, and 270-day-pregnant cows and from parturient cows (3 animals per group) were screened immunohistochemically for expression of the progesterone receptor (PR). During gestation, PR-positive staining was found exclusively in the nuclei of caruncular stromal cells (CSC; maternal part of the placentome) and of caruncular vascular pericytes. In placentomes from parturient cows, occasional positive nuclear staining was also observed in the walls of small caruncular arteries. The percentage of PR-positive CSC increased slightly from 51.8 ± 2.6% on Day 150 to 56.2 ± 5.6% at Day 270 (p < 0.05) and was 58.9 ± 1.8% at parturition. These results suggest that in pregnant cattle, CSC are under the control of P4 of placental rather than luteal origin. Thus, whereas luteal P4 may regulate "coarse" systemic progestational functions in the maternal compartment in the classical hormonal manner, placental P4 may act as a paracrine factor involved in the local regulation of caruncular growth, differentiation, and functions.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
As in many mammalian species, the bovine placenta produces progesterone (P4). Site of P4 synthesis is the trophoblast epithelium, with the binuclear trophoblast giant cells (BNC) being the most active producers [1]. However, bovine placental P4 synthesis contributes only marginally to peripheral maternal plasma levels, and its capacity to maintain pregnancy in the absence of luteal P4 production is restricted to a short phase between about Days 180 and 250 [2–5]. Furthermore, the prepartal decline of peripheral P4 prior to parturition in cattle is a result of luteolysis; the situation is completely different from that in the sheep, where the prepartal decline of P4 results from a switch in placental steroidogenesis from P4 to estrogens [6, 7], though identical prepartal alterations in placental steroid metabolism have also been demonstrated in the cow [8]. A biological need for a P4 source in addition to the corpus luteum during bovine gestation has not been demonstrated unequivocally yet. However, clearly the function of P4 during pregnancy is not restricted to the inhibition of myometrial contractility and closure of the cervix. Thus, additional gestation-related functions influenced by P4 have been identified in other species—for example, the protection of the placenta from maternal immunological attack [9, 10] or the maintenance of the histological integrity of the maternal part of the placenta [11], actions that are probably regulated locally. In cattle, concentrations of P4 in placental tissue rise considerably within the fifth and sixth month of gestation, reaching maximal values in the cotyledons of about 50 ng/g wet tissue in the eighth and ninth month; they decline prior to parturition. However, in parturient cows, cotyledonary P4 concentrations still exceed those determined at midgestation [12, 13].

Therefore, the aims of the study were to identify putative P4 target cells within the bovine placentomes via immunohistochemical localization of progesterone receptors (PR) and to quantitatively monitor the expression pattern in mid and late gestation and at parturition.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Design, Sample Collection, and Fixation

Placentomes were collected from 150-, 220-, 240-, and 270-day-pregnant cows and from parturient cows, forming five experimental groups each consisting of three animals. Maternal concentrations of P4, free and conjugated estrone, and fetal cortisol concentrations were indicative of normal pregnancies. For sample collection, uteri of pregnant cows were removed at slaughter immediately after the animal was stunned by bolt pistol. After opening of the uterus and removal of the fetus, up to five medium-sized placentomes located over the fetus were randomly selected, and cotyledonary arteries were cannulated and perfused with 10% neutral phosphate-buffered formalin. After perfusion, the placentomes were removed from the uteri and immersion fixed for 24 h in the fixative mentioned. Placentomes from the parturient cows were removed in the course of cesarean sections and subjected to immersion fixation only; all three cows delivered a normally developed vital calf and released the placenta within 12 h. Finally, wedge-shaped or trapezoid pieces encompassing the total height of the placentomes were embedded in a paraffin substitute (Histo-Comp; Vogel, Giessen, Germany).

Immunohistochemical Staining Procedure

An indirect immunoperoxidase staining method using clone 10A9 (Immunotech, Hamburg, Germany) as primary antibody and the streptavidin-biotin technique for signal enhancement were applied according to standard procedures. 10A9 is a murine monoclonal antibody elicited against amino acids 922–933, which form the extreme C-terminus of the human PR. Negative controls were set up with the isotype-specific irrelevant monoclonal antibody 7TF–1F5 (Coulter Immunotech Diagnostics, Krefeld, Germany) at a concentration equal to that of the primary antibody. Tissue sections, about 4 µm thick, were mounted on silane-coated slides, deparaffinized by two 15-min changes of xylene, and rehydrated in graded ethanol. For antigen retrieval, the rehydrated sections were preincubated in 10 mM citrate buffer, pH 6.0, for 5 min prior to microwave irradiation (3 times, 5 min each) in preheated citrate buffer in an oven run at 800 W. After a 10-min cooling period, the slides were rinsed in distilled water (2 changes, 2 min each) and PBS, pH 7.2 (3 changes, 5 min each), followed by a treatment with 0.3% hydrogen peroxide in PBS for 20 min in order to quench endogenous peroxidase activity. They were then covered with 10% inactivated horse serum in PBS to block unspecific binding sites. After draining of the blocking reagent, the primary antibody was applied, and the slides were incubated for 20 h in a humid chamber at 4°C. They were then washed with PBS (3 changes, 5 min each), covered with biotinylated horse anti-mouse IgG antibody (Vector Laboratories, Burlingame, CA) diluted 1:200 in PBS, and incubated for 30 min at room temperature. After draining of excess reagent and washing (3 changes, 5 min each) with PBS, the sections were covered with streptavidin-peroxidase complex (Vector) and incubated for 30 min. After washing with PBS (3 changes, 5 min each), the slides were immersed in the substrate solution consisting of 0.05% diaminobenzidine and 0.01% hydrogen peroxide in 50 mM imidazole-HCl buffer, pH 7.1, for 5 min. The sections were then washed, counterstained with hematoxylin, and mounted in Kaisers glycerol-gelatin (Merck KgaA, Darmstadt, Germany).

Qualitative and Quantitative Assessment

From each of the three animals per experimental group, one placentome was randomly chosen, and three sections per placentome were evaluated at a 200- to 400-fold magnification via visual assessment by the same person in direct comparison to the respective negative controls. Quantitative determination of PR-positive caruncular stromal cells (CSC) was performed at a 200-fold magnification. To test for the effect of localization, the sections encompassing the total height of the placentomes were divided into three zones of equal width: a superficial zone close to the chorionic plate (zone I), an intermediary zone (zone II), and a basal zone close to the caruncular stalk (zone III). In each zone the total number and the number of PR-positive CSC were counted in at least two views, arbitrarily chosen, and the percentage of PR-positive CSC was calculated. If the total number of CSC was lower than 200, additional views were analyzed until more than 200 cells per zone had been registered.

Statistical Analysis

The expression of PR in the caruncular stroma was investigated as a function of experimental group and of localization within the placentome (zones I–III). According to the design of the study, a four-factorial ANOVA with partial hierarchic structure (mixed model) was applied using the program BMDP8V (BMDP statistical software [14]) incorporating the following main effects: experimental group (Days 150, 220, 240, 270, parturition—fixed effect), animal nested within group (random effect), section nested within animal (random effect), and zone (fixed effect). The following interactions were incorporated in the model: group x zone (fixed effect), animal (group) x zone (random effect), and section (animal x group) x zone (random effect). Because the interaction group x zone was statistically not significant (p > 0.05), data from zones I–III were pooled, and a one-factorial analysis of covariance with repeated measures in the factor zone (BMDP2V-BMDP statistical software [14]) using arithmetic means over sections was performed to test the trend from Day 150 to Day 270. The group of parturient cows had to be excluded from this analysis because of the inherent variability of the length of pregnancy and hence the day of parturition. For description of the data (see Fig. 2), arithmetic means and standard deviations were calculated for each zone and experimental group from the means of replicated measurements (sections).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Immunolocalization of PR in the Bovine Placentomes

From Day 150 to Day 270 the staining patterns and intensity were very uniform, and no alterations in relation to the stage of gestation could be observed. Representative micrographs from a 220-day-pregnant cow are shown in Figure 1, A–C. Positive reactions were predominantly found in the nuclei of stromal cells of the maternal caruncular septa (Fig. 1, A and B). No morphological differences could be observed between stained and unstained CSC. Also, some vascular pericytes, especially of capillaries located in the free margin of superficial maternal septa (Fig. 1C), exhibited specific nuclear staining. In placentomes from parturient cows (Fig. 1D), a few positive nuclear reactions were additionally found in the walls of small caruncular arteries (Fig. 1E). In these animals, a higher and more homogenous nuclear staining in CSC was observed than in the pregnant animals. No positive reactions could be identified in any other cell type of the caruncle or in the fetal part of the placentome.



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  		FIG. 1. Immunolocalization of PR in bovine placentomes at Day 220 of gestation (A–C) and at parturition (D, E). Irrespective of the stage of gestation investigated and at parturition, positive nuclear staining was detected in CSC of large (A) and fine (A, B) maternal septa. No positive reactions were found in the caruncular epithelium (arrowheads) and in fetal villi (FV, cross-sectioned). C) Additionally, at all stages under investigation, positive nuclear staining was found in capillary-associated pericytes (arrows), predominantly in the free margin of superficial caruncular septa. D) Distinct positive nuclear staining in the broadened caruncular stroma surrounding partly collapsed fetal villi in a parturient placentome. E) Positive immunostaining found in caruncular arteries was confined to placentomes of parturient cows. Bar = 50 µm.

Course of PR Expression in the Caruncular Stroma

The percentage of PR-positive CSC rose slightly from 51.8 ± 2.6% at Day 150 to 58.9 ± 1.8% at parturition (Fig. 2). Analysis of covariance revealed a linear trend between Days 150 and 270 (p < 0.05) with a regression coefficient of 0.048% per day. The percentage of PR-positive CSC was lower in zone II compared to zones I and III (p < 0.005), and this difference was independent from the day of pregnancy or parturition (for interaction group x zone, p > 0.05).



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  		FIG. 2. Percentage (mean + SD) of PR-positive CSC at different stages of gestation and at parturition. Evaluation was performed separately for three zones of equal width: I) superficial zone close to the chorionic plate; II) intermediary zone; III) basal zone close to the caruncular stalk.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
To test for the occurrence of PR in bovine placentomes, a primary antibody elicited against the human PR was used. When compared to observations with two other monoclonal anti–human PR antibodies, 1A6 (Loxo GmbH, Dossenheim, Germany) and BGX-PR88 (BioGenex/DCS, Hamburg, Germany), not only the same staining pattern but also the highest signal-to-noise ratio was obtained with clone 10A9. The fact that the epitope recognized by this clone (extreme C-terminus of the human PR) is identical to the corresponding part of the PR in different species such as the mouse [15], chicken [16], rabbit [17], and rat [18] provides further evidence for the specificity of the method applied.

In cattle the biological functions of placental P4 are still largely unknown. The ability of the bovine placenta to produce P4 was originally recognized by its capacity to maintain pregnancy in the absence of luteal P4 between around Days 180 and 250 [2–5]. Accordingly, Days 150, 220, and 240 were selected as representative for the state immediately prior to, in the middle of, and at the end of this phase; Day 270 was chosen to characterize the state in the phase approaching parturition. However, as indicated by the data obtained, the expression pattern of PR in CSC and capillary pericytes is rather constant, showing only a slight increase (p < 0.05) in the percentage of PR-positive CSC from 51.8 on Day 150 to 56.2 on Day 270. The distribution of PR in the caruncular stroma was not related to the stage of gestation. Yet within placentomes, the percentage of PR-positive CSC was lower (p < 0.005) in zone II compared to zones I and III. Though difficult to interpret, this observation may point to some specific local regulatory mechanisms.

The observation that PR were readily detectable in CSC in spite of the reported presence of high P4 levels [12, 13] is in accordance with the results of Tseng and Zhu [19], who showed that the expression of PR in human endometrial stromal cells is maintained by its ligand whereas in other P4-responsive cell types, especially epithelial cells, PR is down-regulated by progestins [20]. In this respect placental P4 might be more important for the interaction with CSC PR than luteal P4, since the BNC, which are regarded as the main P4 producers among the trophoblast cells [1], enter into almost immediate contact with the putative target cells by invading the caruncular epithelium up to its basal membrane [21]. A direct transfer of placental P4 into the caruncular stroma by migrating BNC has been suggested by Reimers et al. [1]. P4 has been shown to exhibit proliferative and antiproliferative as well as differentiation-inducing effects, obviously depending on the cell type and the cellular context [22–26]. In the endometrium, progestins are commonly regarded as the classical opponents of estrogens, counteracting their proliferation-stimulating effects [27–29]. However, in concert with certain other factors, P4 also stimulates the proliferation of endometrial stromal cells under in vitro conditions [30, 31]; and a role of P4 as a stromal cell mitogen has also been demonstrated in the decidua basalis of the rat, depending on gestational age [26]. As PR are highly expressed in CSC of parturient cows, the placentomes are apparently P4-sensitive at parturition. Thus, problems concerning the course of parturition or shedding of the placenta may result from cases of inappropriate withdrawal of local P4. This suggestion is supported by results obtained in cows in which parturition was induced with an antiprogestagen, after which—in contrast to what occurred with the use of prostaglandins or glucocorticoids—no increased incidence of retained placentae was reported [32]. PR were also detected in capillary-associated pericytes and in arterial walls, suggesting that P4 may also be involved in the local regulation of caruncular angiogenesis and/or blood flow by either direct or indirect mechanisms. That the detection of PR in arterial walls was confined to parturition may suggest a down-regulation during the second half of pregnancy and an up-regulation concomitant with changes of placental steroidogenesis, leading to the prepartal increase of free estrogens that were characterized in a previous study using placentomes from cows at Days 220 and 270 of pregnancy and at parturition [8, 13]. The necessity of high estrogen concentrations for the induction of PR in uterine arteries has been demonstrated in rabbits [33].

In conclusion, PR in the bovine placentomes are expressed in CSC and in caruncular vascular cells that are located in close proximity to the site of ligand production. Thus, these cells seem to be under the control of placental rather than luteal P4. This suggests a role of placental P4 as a paracrine factor involved in the regulation of placental growth, differentiation, and functions.


   ACKNOWLEDGMENTS
 
The authors acknowledge the assistance of Dr. Klaus Failing, Institute of Veterinary Physiology, section biomathematics, Justus-Liebig-University, Giessen, with the statistical evaluation of the data, and the assistance of Ruth Klein with the photographic documentation.


   FOOTNOTES
 
1 Supported by the German Research Foundation (DFG) grant SCHU 1195/1–1 and the Hilde und Ewald Berge-Stiftung. Back

2 Correspondence: Gerhard Schuler, Klinik für Geburtshilfe, Gynäkologie und Andrologie der Groß- und Kleintiere mit Tierärztlicher Ambulanz, Justus-Liebig-Universität Giessen, Frankfurter Strasse 106, D-35392 Giessen, Germany. FAX: 49 641 29328; gerhard.schuler{at}vetmed.uni-giessen.de Back

Accepted: May 6, 1999.

Received: January 5, 1999.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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